The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.

A N Belozersky Institute of Physico Chemical Biology Moscow State University Russia

Arthropoda Department Center for Taxonomy and Evolutionary Research Zoologisches Forschungsmuseum Alexander Koenig Bonn Germany

B CUBE Center for Molecular Bioengineering Technische Universität Dresden Germany

Berkeley Bioinformatics Open source Projects Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley California

Biochemistry Department University of Otago Dunedin New Zealand

Center for Bioinformatics Tübingen University of Tübingen Germany

Center for Molecular Biodiversity Research Zoologisches Forschungsmuseum Alexander Koenig Bonn Germany

Center for Translational Biodiversity Genomics Frankfurt Germany

Center of Life Sciences Skolkovo Institute of Science and Technology Russia

Computational Biology Group Leibniz Institute on Aging Fritz Lipmann Institute Jena Germany

Department of Biological Sciences Oakland University Rochester

Department of Biological Sciences University of Cincinnati

Department of Biological Sciences Wayne State University Detroit

Department of Biology Georgia Southern University Statesboro

Department of Biology University of Copenhagen Denmark

Department of Biology University of Rochester

Department of Ecology and Evolution University of Lausanne Switzerland

Department of Entomology Purdue University West Lafayette

Department of Environmental Science Policy and Management College of Natural Resources University of California Berkeley

Department of Evolutionary Biology and Ecology Institute of Biology 1 Albert Ludwig University Freiburg Germany

Department of Evolutionary Neuroethology Max Planck Institute for Chemical Ecology Jena Germany

Department of Genetic Medicine and Development University of Geneva Medical School Switzerland

Department of Neuroscience The Scripps Research Institute Jupiter Florida

Department of Psychiatry and Behavioral Neuroscience University of Chicago

Division of Evolutionary Biology Faculty of Biology Ludwig Maximilians Universität München Planegg Martinsried Germany

Division of Medical Zoology Department of Infection and Immunity Jichi Medical University Yakushiji Shimotsuke Japan

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Praha 6 Suchdol Czech Republic

Genomics Aotearoa and Biochemistry Department University of Otago Dunedin New Zealand

Graduate Institute of Biomedical Electronics and Bioinformatics National Taiwan University Taipei Taiwan

Groningen Institute for Evolutionary Life Sciences University of Groningen The Netherlands

Human Genome Sequencing Center Department of Human and Molecular Genetics Baylor College of Medicine Houston Texas

INRAE CNRS IRD UPEC Univ P7 Institute of Ecology and Environmental Sciences of Paris Sorbonne Université Paris France

INRAE CNRS IRD UPEC Univ P7 Institute of Ecology and Environmental Sciences of Paris Sorbonne Université Versailles France

INSA Lyon INRAE BF2I UMR0203 Université de Lyon Villeurbanne France

Insect Genome Research and Engineering Unit Division of Applied Genetics Institute of Agrobiological Sciences NARO Owashi Tsukuba Japan

Institute for Evolution and Biodiversity University of Münster Germany

Institute for Insect Biotechnology University of Gießen Germany

Institute of Evolutionary Biology and Ecology Zoology and Evolutionary Biology University of Bonn Germany

Institute of Molecular Biology and Biotechnology Foundation for Research and Technology Hellas Heraklion Crete Greece

Lead Contact

Max Planck Institute of Immunobiology and Epigenetics Freiburg Germany

School of Biology Faculty of Biological Sciences University of Leeds United Kingdom

School of Life Sciences College of Liberal Arts and Sciences Arizona State University

Swiss Institute of Bioinformatics Geneva Switzerland

Swiss Institute of Bioinformatics Lausanne Switzerland

Transgenic Silkworm Research Unit Division of Biotechnology Institute of Agrobiological Sciences National Agriculture and Food Research Organization Owashi Tsukuba Japan

USDA Agricultural Research Service Center for Grain and Animal Health Research Manhattan Kansas

USDA ARS National Agricultural Library Beltsville Maryland

Zoological Institute University of Hamburg Germany

Zoology Department University of Cambridge United Kingdom

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